CITATION

Denisenko, S.G., J.M. Grebmeier, and L.W. Cooper. 2015. Assessing bioresources and

standing stock of zoobenthos (key species, high taxa, trophic groups) in the Chukchi

Sea. Oceanography 28(3):146–157, http://dx.doi.org/10.5670/oceanog.2015.63.

DOI

http://dx.doi.org/10.5670/oceanog.2015.63

COPYRIGHT

This article has been published in Oceanography, Volume 28, Number 3, a quarterly

journal of The Oceanography Society. Copyright 2015 by The Oceanography Society.

All rights reserved.

USAGE

Permission is granted to copy this article for use in teaching and research.

Republication, systematic reproduction, or collective redistribution of any portion of

this article by photocopy machine, reposting, or other means is permitted only with the

approval of The Oceanography Society. Send all correspondence to: info@tos.org or

The Oceanography Society, PO Box 1931, Rockville, MD 20849-1931, USA.

OceanographyTHE OFFICIAL MAGAZINE OF THE OCEANOGRAPHY SOCIETY

DOWNLOADED FROM HTTP://WWW.TOS.ORG/OCEANOGRAPHY

Oceanography | Vol.28, No.3146

RUSSIAN-AMERICAN LONG-TERM CENSUS OF THE ARCTIC

Assessing Bioresources and Standing Stock of Zoobenthos (Key Species, High Taxa, Trophic Groups)

in the Chukchi Sea

By Stanislav G. Denisenko, Jacqueline M. Grebmeier, and Lee W. Cooper

Oceanography | Vol.28, No.3146 Photo credit: Mark Dennett

Oceanography | September 2015 147

and distribution of ecological communi­ties, including energy flows (Piraino et al., 2002). Biological metrics include faunal biomass, abundance, productivity, and function in the ecosystem.

The Chukchi Sea’s marine resources (Figure  1a) are not harvested commer­cially, although local people fish, hunt marine mammals, and harvest benthic invertebrates for their own use. Locally potential harvested benthic species in the Chukchi Sea include the bivalves Mya, Serripes, Mytilus, Chlamys, and Macoma; several carnivorous gastro­pods from the genera Buccinum and Neptunea; the snow crab Chionoecetes opilio; and sea urchins from the genus Strongylocentrotus. However, the exact quantity of this bio resource available for harvesting is not known.

Other bioresources include plants and animals consumed by marine mammals, fishes, and birds. The Chukchi Sea attracts large numbers of walruses, seals, bow­head and gray whales, and eiders that are either resident to the area or migrate to specific regions every year to feed, some on benthic prey. Some of these benthic species are listed in the Red Data Book

of the Russian Federation (Illiashenko and Illiashenko, 2000) and/or are pro­tected under the Endangered Species Act of the United States.

Among the marine mammals, the main consumers of benthos in the Pacific Arctic region are Pacific walruses and gray whales (Moore et al., 2014). Walruses feed on bivalves and gastropods, crustaceans, worms, and ascidians (Krylov, 1971; Sheffield and Grebmeier, 2009), while gray whales prefer crustaceans, especially amphipods, and other high biomass ben­thic species (Blokhin and Pavluchkov, 1996; Highsmith et al., 2006).

Benthic biomass in the north­ern Pacific Ocean increases northward from the Sea of Japan to the Bering Sea (Zenkevich, 1951; Shuntov, 2001), increasing to high values in the south­ern Chukchi Sea (Makarov, 1937; Sirenko and Koltun, 1992; Grebmeier et al. 2006). A considerable proportion of this benthic fauna is represented by mollusks, crus­taceans, polychaetes, sipunculid worms, echinoderms, and ascidians, and known regions of high benthic prey abundance attracts walruses, seals, whales, and birds to these areas to feed.

In order to identify and quantify the bioresources of the Chukchi Sea, we pres­ent a general assessment of the key species of benthic invertebrates, based on quan­titative grab samples of macrobenthic fauna. This study also evaluates the biore­source potential of the major higher taxa components (at the level of class or phy­lum) and associated trophic groups. We present (1) key species identified by their contributions to the total zoobenthos biomass, and (2) spatial distribution of

INTRODUCTIONWith increasing depletion of commercial fisheries, the number of newly harvested marine species is on the rise. Thus, there is an immediate need to estimate all avail­able biological resources (termed bio­resources in this paper) used by humans, including food for consumption, forage feed for domestic animals, and indus­trial raw materials. These new resources and their potential economic importance require a quantitative assessment of the total biomass (abundance) and the spatial distribution of the resource base.

In order to monitor and study the long­term dynamics of zoobenthic pop­ulations, it is necessary to analyze the spatial distributions of those species or higher­level taxa that contribute most to the total biomass in an area of inter­est. As a rule, the number of such spe­cies in each Arctic sea does not exceed 20 (Denisenko, 2004), with 50% of the zoo­benthos biomass being formed by fewer than 10 species. These few can be con­sidered the “key species” influencing the structure and function of the associated ecosystems and they have key roles in controlling the structure, development,

ABSTRACT. We describe total standing stock and spatial biomass distribution of the key macrofaunal species, as well as the main taxonomic and trophic groups of zoobenthos, in the Chukchi Sea based on data collected over the period 1986–2012. The dominant species, ranked by biomass, are the bivalves Macoma calcarea, Ennucula tenuis, Astarte borealis, Nuculana radiata, and Yoldia hyperborea; the sipunculid, Golfingia margaritacea; the polychaete Maldane sarsi; and the sea cucumber Psolus peroni. We discuss the influence of bottom sediments and water masses on zoobenthos bioresources and standing stock and present a hypothesis for the mechanism that facilitates the phenomenon of very high benthic biomass in the southern Chukchi Sea. The relationship between biomass of filter feeders and deposit feeders indicates that the Chukchi Sea should be classified as a eutrophic marine system.

FIGURE 1. (a) Bathymetry of the Chukchi Sea, and (b) proportion of silt + mud content (%) in the bottom sed-iments. Modified after Kosheleva and Yashin (1999); Grebmeier (2012)

a b

Oceanography | Vol.28, No.3148

was necessary in order to compare differ­ent biomass values in the same local max­ima or minima. A significant difference between these values can considerably decrease Pearson correlation even when the spatial distributions under compari­son are visually very similar.

Organism feeding types were also used in the analysis and are based on previously published categorizations (Kuznetsov, 1980, 1986).

RESULTSComparison of benthic faunal biomass, statistically weighted by area at each sta­tion, revealed eight macrofaunal spe­cies contributing up to 50% of the total zoobenthos bioresources of the Chukchi Sea (Table 1). Five of these species were bivalve mollusks: Macoma calcarea, Ennucula tenuis, Astarte borealis, Nuculana radiata, and Yoldia hyperborea. Of these, M.  calcarea was the most important and abundant, with a total bio­mass (i.e.,  bioresources) several times greater than those of any other bivalve species evaluated separately.

The zoobenthos biomass and the five key bivalve species were unevenly dis­tributed. The highest values of total macrofaunal biomass were observed in the southern and northwestern areas of the sea (Figure 3a), and М. calcarea had the highest biomass of all species in the southern and the southwestern areas (Figure  3b). The highest biomass val­ues of a second bivalve, E.  tenuis, also occurred in the southwestern portion of the Chukchi Sea (Figure  3c). The high­est biomass of A. borealis was recorded in the northern part of the sea as well as in the south, in Koluchin Bay and Kotzebue Sound (Figure 3d). The major settlements of N.  radiata extended toward the west­ern part of the Chukchi Sea (Figure 3e). High biomass values of the sipunculid Golfingia margaritaceum were mostly recorded in northern and the northeast­ern areas (Figure 3f).

Significant Spearman correlations indi­cated some degree of spatial distribution similarity, by biomass, of М. calcarea and

months in formalin. Station­wise species lists of abun­

dance and biomass for all data were pooled into a common data set. Based on these files, maps of the spatial distribu­tions of species, taxonomic groups, and trophic groups were constructed using Ocean Data View 4.7.3 (Schlitzer, 2015). The total benthic biomasses of compo­nents were displayed spatially using geo­statistical interpolations performed with Surfer  8 and MapViewer 7.2 (http://www.goldensoftware.com). Kriging, with a spherical variogram and search ellipse with a radius of –5° longitude and –1.8° latitude (Software Surfer, v8), was used as a universal interpolator. These parameters were experimentally found to be optimal with respect to the devia­tion of calculated values from the actual data. On average, the calculated deviation made up not more than 10% of the actual benthic faunal biomass found at the study sites. The map surface areas were based on the northern border of the Chukchi Sea being located along 72°30'N°, with a total area of ca. 335,000 km2. The west­ern border was located to the north of Wrangel Island along 180°W and further to the south from Cape Blossom to Cape Yakan. The eastern border was located along 158°W (Figure 1).

In order to assess the similarity of spa­tial distributions of individual species, taxonomic groups, and trophic groups, the Spearman rank coefficient rather than the Pearson correlation was used. This

these species using geographical imagery, together with an evaluation of the quanti­tative distribution of the dominant benthic taxa and their trophic levels in the food web. A companion paper by Grebmeier et  al. (2015b) in this special issue dis­cusses total benthic community composi­tion of benthic macro­ and megafauna in the context of environmental factors.

MATERIALS AND METHODSThis study was based on quantitative zoo­benthos samples collected at 640 stations in the Chukchi Sea by specialists from the Zoological Institute of the Russian Academy of Sciences and scientists from the University of Alaska Fairbanks and the University of Maryland Center for Environmental Science over the period 1976–2012 (Figure  2). Macrofauna were collected during multiple cruises in both Russian and US waters through programs that included the Russian­American Long­term Census of the Arctic (RUSALCA). Three to five replicates (with a few two­replicate stations) were col­lected using either a 0.25 m2 Okean grab or a 0.1 m2 van Veen grab, with sedi­ment sieved over primarily 1 mm screens (a few over 0.8 mm screens). The remain­ing macrofauna were preserved in 4–10% seawater formalin buffered with borax or hexamethylenetetramine. Macrofauna were later identified to genus or spe­cies levels (or to the lowest taxon pos­sible), with the taxa subsequently counted and weighed after three to four

FIGURE 2. Locations of 640 sample stations in the Chukchi Sea collected on (a) Russian (light cir-cles) and American expeditions (dark circles) from 1986 to 2012, and (b) locations of the stations collected before the year 2000 (light circles) and after 2000 (dark circles). Note that by conven-tion, the northern border of the Chukchi Sea in the west extends to 75°N, with an areal extent of the sea of 595,000 km2 (Anonymous, 1985).

a b

Oceanography | September 2015 149

E. tenuis (S = 0.51), and of A.  borealis and G.  margaritacea (S = 0.52). Bivalves clearly dominate in biomass compared with the other large macrofaunal taxa in the Chukchi Sea (Table  2). They made up more than 50% of the zoobenthos bioresources by both wet and dry weight biomass. Even considering that the cal­cium carbonate shell accounts for about 30–50% of the molluskan wet bio­mass (Alexey V. Golikov, Kazan Federal University, pers. comm., 2015; Stoker, 1978; Brey, 2001; Denisenko, 2013), bivalves are still the dominant taxa by biomass. This finding was also supported by recalculat­ing the wet biomass on an organic carbon basis (Stoker, 1978; Grebmeier, 2012). The contribution of other taxonomic groups was an order of magnitude lower than that of bivalves (see Table 2). Polychaetes accounted for ~11% of total zoobenthos bioresources, as did echinoderms (holo­thurians and sea urchins).

The distribution of bivalve biomass (Figure  4a) resembled that of the total zoobenthos biomass (see Figure  3a). However, the biomass values for Bivalvia were much lower in the northwestern and, especially, in the northeastern part of the sea relative to the high southern Chukchi Sea biomass values, although they can be regionally important. Polychaetes dom­inated locally in Herald Canyon in the north (Figure 4b), while significant com­munities of holothurians were observed near Wrangel Island (Figure  4c). In the eastern part of the Chukchi Sea as well as in Bering Strait, dense settlements of sea urchins were found alongside those of holothurians (Figure 4d).

Ascidians (Figure  5a), barnacles (Figure 5b), amphipods (Figure 5c), along

with sea urchins, mostly formed biomass aggregations in the southern and north­ern parts of the Chukchi Sea, where water

dynamics were the greatest. Judging from the location of the local biomass max­ima of these groups, these varying taxon

TABLE 1. Contribution of different species into total bioresources (by mass, tons) and total specific biomass (g wet weight m–2) of zoobenthos over the whole Chukchi Sea. R% = Proportion of the total bioresources. R,t = Bioresources (tons). B = Average specific total biomass (g wet weight m–2) within regions. BErr = Statistical error of the average specific total biomass.

Species Feeding mode R% R,t(tons)

B(gww m–2)

BErr(gww m–2)

Macoma calcarea* Filter/Surface Deposit Feeder 9.4 8,269,498 92.8 16.3

Ennucula tenuis Surface Deposit Feeder 7.4 6,492,153 33.2 5.8

Astarte borealis Filter Feeder 4.6 4,087,168 89.0 10.4

Golfingia margaritacea Subsurface Deposit Feeder 2.7 2,384,643 62.3 5.7

Nuculana radiata Surface/Subsurface Deposit Feeder 7.6 6,740,267 35.8 5.6

Yoldia hyperborea Surface/Subsurface Deposit Feeder 5.9 5,215,108 18.1 2.7

Maldane sarsi Subsurface Deposit Feeder 8.2 7,269,498 25.9 2.4

Psolus peroni Filter Feeder 6.2 5,492,154 143.7 7.8

Others 48.0 42,373,638

Total 100 88,324,127 592.5 39.7

*All mollusks from the family Tellinidae were considered to be an intermediate group between filter feeders and surface deposit feeders (Kuznetsov, 1986).

(a) Total zoobenthos (d) Bivalve Astarte borealis

(b) Bivalve Macoma calcarea (e) Bivalve Nuculana radiata

(c) Bivalve Ennucula tenuis (f) Sipunculid Golfingia margaritacea FIGURE  3. Biomass (g wet weight m–2) distri-bution of (a) total zoobenthos; the bivalves (b) Macoma calcarea, (c) Ennucula tenuis, (d) Astarte borealis, and (e) Nuculana radiata; and the (f) sipunculid Golfingia margaritacea in the Chukchi Sea from 1986–2012. Note the higher vertical scale of Macoma calcarea bio-mass compared with the biomass of other species in the Chukchi Sea that are shown in subsequent maps.

Oceanography | Vol.28, No.3150

settlements did not overlap each other. Due to this separation of groups, the sig­nificant Spearman correlation coeffi­cients, which indicate similarity of the spatial distribution of fauna by biomass, were only obtained for Ascidiacea and Echinoidea (S = 0.77).

Filter feeders (suspension feeders) pre­dominate overall for much of the spatial extent of the Chukchi Sea. Their propor­tion exceeded 44% of the total biomass, making up approximately 40 million tons, with an average wet biomass of 141 g m–2 (Table 3). The proportion of deposit feed­ers (including both surface and subsur­face deposit feeders) is about equal to the filter feeders, making up 45.2% of the overall biomass or approximately 40 mil­lion tons. The bioresources proportion of surface deposit feeders to subsurface deposit feeders was 3:2. Omnivorous and predatory species contributed less than 10%, and made up 7.5 million tons. On the whole, the average biomass value of each trophic group was better correlated with its individual bioresource value than biomass of the large taxa or the key spe­cies groups with their individual biore­source values (see Tables 1, 2, and 3).

The spatial distribution of trophic groups shows a tendency toward replace­ment of communities where filter feeders dominate (mostly in the southernmost and northwesternmost parts; Figure 6a) with communities in which surface deposit feeders dominate (in the northeastern and southwestern parts; Figure 6b). Slow­moving subsurface deposit feeders domi­nate in the northeastern Alaska Chukchi coastal waters, around Hanna Shoal, and to the east and south of Wrangel Island (Figure  6c) within silty­clay sedi­ments (Figure 1b). The highest biomass of predators coincides partly with the total zoobenthos biomass.

DISCUSSIONBenthic Communities Defined by Biomass Spatial Patterns Visual or computerized demarcation of benthic communities based on the results of clustering or ordination is the most

TABLE 2. Contribution of higher taxa into total bioresources (by mass, tons) and total specific weight (g wet weight m–2) of zoobenthos in the Chukchi Sea. R% = Proportion of the total bioresources. R,t = Bioresources (tons). B = Average specific total biomass (g wet weight m–2) within regions. BErr = Statistical error of the average specific total biomass.

Higher taxa R% R,t (tons) B (gww m–2) BErr (gww m–2)

Bivalvia 54.1 47,777,578 169 32.4

Polychaeta 11.0 9,722,948 36.9 4.2

Holothuroidea 6.8 5,966,515 47.7 15.6

Echinoidea 4.2 3,687,117 127 41.7

Ascidiacea 3.8 3,363,200 34.1 8.4

Sipunculida 3.1 2,697,232 25.2 3.1

Cirripedia 2.6 2,311,321 31.1 9.7

Amphipoda 2.4 2,100,767 8.1 1.7

Anthozoa 2.4 2,090,435 20.1 3.9

Others 9.7 8,607,014

Total 100 88,324,127 592.5 39.7

Note: All mollusks from the family Tellinidae were considered to be an intermediate group between filter feeders and surface deposit feeders (Kuznetsov, 1986).

(a) Bivalve mollusks

(b) Polychaetes

(c) Holothurians

(d) Sea urchins

FIGURE 4. Biomass distribution (g wet weight m–2) of (a) bivalve mollusks, (b) polychaetes, (c) holo-thurians, and (d) sea urchins in the Chukchi Sea from 1986–2012.

TABLE 3. Contribution of different trophic groups into total bioresources and total biomass of zoo-benthos in the Chukchi Sea. R% = Proportion of the total bioresources. R,t = Bioresources (tons). B = Average biomass in settlements, g m–2 of wet conserved biomass; BErr = Statistical error of the average biomass.

Trophic mode R% R,t (tons) B (gww m–2) BErr (gww m–2)

Filter feeders 44.2 39,035,073 153 21.3

Surface deposit feeders 26.2 23,176,154 202 10.1

Subsurface deposit feeders 19.0 16,819,154 59.2 4.5

Carnivorous 6.2 5,448,669 39.7 5.3

Omnivorous 2.5 2,248,628 37.0 4.9

Scavengers 0.1 80,468.4 0.48 0.12

Unclear 1.7 1,515,981

Total 100 88,324,127 592.5 39.7

Note: All mollusks from the family Tellinidae were considered to be an intermediate group between filter feeders and surface deposit feeders (Kuznetsov, 1986).

Oceanography | September 2015 151

common method used for local zonation of marine benthic biota and for compar­ing qualitative and quantitative character­istics of zoobenthos in various regions and over temporal periods (Denisenko, 2007). Most researchers define a “biological community” as the combination of popu­lations of organisms interacting with each other and with the environment in space and time (Möbius, 1877; Whittaker, 1975; Bigon et al., 2006). However, this defini­tion is somewhat vague because the com­munities usually have no distinct bor­ders but rather transition into each other imperceptibly (Pianka, 1994). Besides, the use of different approaches and software yields different, and often not compara­ble, results describing the dominance of a given group in a given area.

Certain methods can be limiting in their demarcation of benthic communi­ties because of assumptions that species always have the same quantitative rep­resentation in communities (Vorobyev, 1949; Clarke and Warwick, 2001). The possibility of detecting changes in the abundance and biomass of populations can be obscured, although long­term fluctuations and quantitative indices of many benthic invertebrates (Pearson and Rosenberg, 1978; Gerasimova and Maksimovich, 2000; Kortsch et al. 2012; Denisenko, 2013), plankton (Krause­Jensen et al., 2012), and fish (Klyashtorin and Lubushin, 2005) are well known. As a result, comparing the distributions of the so­called communities in different marine areas and for different research periods might be reduced to a compari­son of the degree of dominance of a few key species, such as indicated in our pres­ent study. A cyclic decrease or increase in the abundance or biomass of these species, caused by any environmental changes, may result in a misclassification of communities on the basis of species dominance (Denisenko, 2013).

Our research indicates that the most abundant species can also dominate by biomass in benthic communities (Table 1; Denisenko, 2004, 2007; Sirenko et  al., 2009; Grebmeier et  al., 2015a). These

species often serve as the major food source for numerous benthic­feeding mammals and birds. Therefore, the assessment of macrobenthos biomass should be based on direct calculations of the quantitative spatial distributions of those key species, higher taxa, and trophic groups that dominate the bio­mass (i.e.,  bioresources) in a study area. The importance of these species as future human resources may better be assessed by a simple interpolation of biomass on

a map. In contrast to various methods of “community” classification, includ­ing visual recognition of dominant spe­cies, our simplified approach will more directly facilitate comparative analysis in the future. In addition, using interpola­tion approaches, the outliers on the maps are to some degree smoothed, which compensates for possible sampling errors and the mosaic nature of organismal dis­tributions on the seafloor.

Using this approach of statistically

(d) Sea anemones

(c) Amphipods

(b) Barnacles

(a) Ascidians

FIGURE 5. Biomass distribution (g wet weight m–2) of (a) ascidians, (b) barnacles, (c) amphipods, and (d) sea anemones in the Chukchi Sea from 1986–2012.

(d) Predators

(c) Subsurface deposit feeders

(b) Surface deposit feeders

(a) Filter feeders

FIGURE 6. Biomass distribution (g wet weight m–2) of (a) filter feeders, (b) surface deposit feeders, (c) subsurface deposit feeders, and (d) predators in the Chukchi Sea from 1986–2012.

Oceanography | Vol.28, No.3152

Sirenko and Gagaev, 2007) coincide with the locations of known particle deposi­tions sites to the north of Bering Strait (Sirenko and Koltun, 1992; Cooper et al., 2005; Grebmeier et  al. 2006; Pisareva et al., 2015, in this issue). This high ben­thic biomass zone may result from slow­ing current speeds (Ratmanov, 1937) and possible cyclonic features that are pres­ent in the autumn (Pickart et  al., 2013; Figure  7). A nearly continuous input of nutrients through Bering Strait allows the phytoplankton community to func­tion actively throughout the period of sufficient light and to provide the under­lying sediments with a continuous supply of fresh phytodetritus, the major source of food for benthic invertebrates. In con­trast, in other Arctic regions, spring development of phytoplankton blooms is subsequently inhibited by depletion of nutrients in the surface layers of stratified water columns (Sakshaug 2004). Thus, during most of the season when light is available, the sinking of phytodetritus to the bottom in these other regions is weak, thus limiting the production and biomass of underlying zoobenthic communities.

The exact mechanism for this strong pelagic­benthic coupling is uncertain, but its role in the annual formation of a zone of high benthic biomass in the southern Chukchi Sea is critical. The existence of periodic cyclonic type cir­culation is supported by hydrographic section data. However, we disagree with Ratmanov’s (1937) interpretation that the cyclonic gyre arises from the inter­action of northward­flowing Pacific water and a southwest­flowing East Siberian Current. More recent data indicate a vari­able, more ephemeral flow from the East Siberian Sea along the Chukchi Sea coast to the southern Chukchi Sea (Münchow et  al., 1999; Weingartner et  al., 2005). It is more likely that the greater depth to the northwest helps facilitate a cyclonic­ type circulation in the upper portion of Central Valley. This alternative mech­anism would result in enrichment of the photosynthetic water layer by nutri­ents and enhanced carbon export to the

weighted spatial benthic data analysis, it was determined that 75–80% of the total macrofaunal biomass of the Barents Sea during a defined study period was made up of 15–20 taxa, with 7–10 species mak­ing up 40–50% of the total benthic bio­mass (Denisenko, 2004; Wassmann et al., 2006). By comparison, using the same statistical methods with a large suite of data in the Chukchi Sea, we found fewer taxa were dominant, with eight species making up nearly 50% of the total ben­thic biomass (or bioresources).

Environmental Factors Influencing Benthic Community StructureThe composition and biomass of macro­benthos in the Chukchi Sea are deter­mined by the locations of water masses and associated frontal zones, cur­rents, seawater temperature and salin­ity, and the content of organic carbon in the sediments and in the water col­umn (Grebmeier et al., 1989; Feder et al., 2005, 2007). Seafloor topography, com­bined with the current regime, is the crit­ical factor influencing the characteristics of bottom sediments and ultimately the associated concentration of organic car­bon in them (Gorshkova, 1975; also see Pisareva et al., 2015, in this issue).

Comparison of the distributions of bottom sediment grain size, total benthic biomass, and the biomass of the domi­nant taxa in the Chukchi Sea shows that sediments with similar contents of sand, silt, and clay fractions are the most favor­able for the development of zoobenthos settlements, and they are also character­ized by a large amount of bioresources (see Figures  1b and 3a). Faunal abun­dance and availability of food have major influences on the quantitative develop­ment of the zoobenthos. Average annual primary production in the Chukchi Sea varies from 20 to 200 gC m–2 (Sakshaug, 2004; Codispoti et  al., 2013). Regions with increased concentrations of sus­pended and freshly deposited organic matter depend on the intensity of the nutrients supplied via currents from the Bering Sea as well as locations of frontal

water masses (Grebmeier, 1993, 2012) and of the ice edge (Denisenko, 2002).

The Chukchi Sea is three to four times shallower (average depth of 50 m) than the western seas of the Russian Arctic, and the amount of detritus deposited on the bot­tom from the surface layers of the water is thus higher. The shallow depths of the Chukchi Sea ensure abundant food is sup­plied to benthic invertebrates (Grebmeier et al., 1989; Grebmeier, 1993; Iken et al., 2010). As a result, very high zoobenthos biomass, exceeding 1 kg m–2, is formed even in the open sea areas (see Figure 3a). The bottom of the Chukchi Sea is a flat­tened plain that dips slightly toward the center and has an average depth of less than 80 m. Contrary to other Arctic seas, there is a distinct dependence of zoobenthos distribution on phytoplankton biomass (Grebmeier, 1993, 2012). The bottoms of other Arctic seas (e.g.,  the Barents Sea) are highly uneven and characterized by a considerable (hundreds of meters) depth range between shallow banks and deep channels (average depth of 250 m). Thus, different areas of the seafloor receive dif­ferent amounts of biologically degraded organic matter produced by phytoplank­ton. In the Chukchi Sea, where depth vari­ations are much less pronounced, there is tighter pelagic­benthic coupling of upper water column production to the under­lying benthos. However, a recent synthesis by Grebmeier et al. (2015a) found a defi­nite latitudinal decline in export produc­tion and benthic biomass overall from the southern to the northern Chukchi Sea due to reduced levels of primary production and water mass variability. The complex water mass structure and current flow in the northern Chukchi Sea, with its shoals and canyons, adds to the heterogeneity of ecosystem dynamics and underlying ben­thic populations in that region.

Potential Mechanisms for Maintenance of High Benthic Biomass ZonesThe biomass maxima of benthic inverte­brates recorded in the southern part of the Chukchi Sea (Grebmeier et al., 2006;

Oceanography | September 2015 153

underlying sediments that support the high bivalve biomass in this region. This southern Chukchi Sea gyre may exist as a persistent feature, regardless of the pres­ence or absence of an opposed current, with only the size of the cyclonic gyre varying with variable current flows of the different water masses in the region.

Functional Feeding GroupsOur schematic maps indicate that the Chukchi Sea can be separated into two regions of almost equal size: (1) southern and northwestern with an active current regime, and (2) northern with slower, but more variable, near­bottom hydro­dynamics (Figure 1). This hydrodynamic separation is reflected in the distribution of suspension feeders vs. deposit feed­ers, whose nearly equal bioresources are divided in distribution and follow the hydrodynamic regimes (also see Pisareva et al., 2015, in this issue).

Hydrodynamics are most intense in the southern area just north of Bering Strait, along the Alaska and Chukotka coastlines, and within Herald Canyon to the east of Wrangel Island. Coarse sandy deposits (Figure 1b) on the seafloor in this region are better suited for attached organisms such as ascidians, barnacles, and several filter­feeding amphipods (Figure  5a–c). These areas are characterized by moder­ately high values of zoobenthos biomass (Figure  3a). The presence of suspension feeders indicates high organic matter con­tent in the near­bottom water layer. The suspended particulate matter may origi­nate both autochthonously, resulting from the development of local phytoplank­ton, and allochthonously, as organic mat­ter transported into the Chukchi Sea via the Bering Strait inflow. Surface deposit feeders generally dominate in the upper Herald Valley and in the south central Chukchi Sea, with decreasing biomass to the northwest (Figure 6b).

The prevalence of subsurface deposit feeders in the northeastern and northern Chukchi Sea areas indicates a horizontal input of fresh organic matter. This func­tional group is especially characteristic of

eastern areas (Feder et al., 2005; Blanchard et  al., 2013a,b; Blanchard and Feder, 2014) and depends on the transfer of the fresh organic matter from southern areas (Grebmeier et al., 2015a). A second region of organic matter accumulation is observed to the northwest in Herald Canyon (Kosheleva and Yashin, 1999). Increased concentrations of organic mat­ter in the near­ bottom water layer along the canyon slopes ensure ample develop­ment of filter­feeding organisms, while the accumulation and burial of organic matter in the bottom sediments provide food for subsurface deposit feeders.

Finally, the highest biomass of pred­ators (Figure 6d) coincides with areas of highest zoobenthos biomass (i.e.,  south­east Chukchi Sea and in Herald Canyon; Figure  3a). The distributions of Chukchi Sea trophic groups identified in this study, and the fact that they are determined by environmental factors, agree well with the results of earlier studies carried out in the eastern part of the sea (Feder et al., 2005, 2007). In the southern Chukchi Sea, as in the Pechora Sea, the shallow part of the Barents Sea, the distribution of fil­ter feeders was not just confined to the coastal areas, as occurs in the Barents Sea (Denisenko, 2007), but they were often most abundant in the offshore regions.

Observations of almost equal propor­tions of suspension and deposit feed­ers are consistent with the findings of Neiman (1961), who concluded that such a distribution of trophic zones is char­acteristic of seas with a broad and gen­tly sloping continental shelf. According to Neiman (1988), the trophic structure of zoobenthos in the Chukchi Sea, on the whole, may be considered eutrophic. Such a structure usually develops due to a weakly balanced trophic cycle in the pelagic community where zooplankton are insufficient to consume the available organic carbon (Grebmeier et al., 2006).

Indeed, all the key zoobenthos spe­cies of the Chukchi Sea have a broad or a cosmopolitan boreal­Arctic distribu­tion. Astarte borealis may reach an age of 26 years (Denisenko, 1997), Macoma

calcarea 15–17 years (Petersen, 1978; Denisenko, 1997), Yoldia hyperborea 13 years (Rusanova, 1963), Golfingia margaritacea at least six years (Denisenko, 2006), and Maldane sarsi at least four years (Denisenko, 2006). A limited, but detailed, study of the growth rate of Y. hyperborea (Box 1) indicates that bivalve growth rate is tied to climate forcing parame­ters, such as the Arctic Oscillation; thus, the future stability of bivalve populations may change. Since bivalves are a major bioresource in the Chukchi Sea for upper

(a) 1990

(b) 2004

(c) 2009

(d) 2012

FIGURE  7. Distribution of surface sea-water temperatures in August/September of (a) 1990, (b) 2004, (c) 2009, and (d) 2012 in the Chukchi Sea.

Oceanography | Vol.28, No.3154

Box 1. Relationship of Growth Patterns in a Chukchi Sea Bivalve Population to the Arctic Oscillation

By Stanislav G. Denisenko and Vladimir V. Skvortsov

Forty live specimens of Yoldia hyperborea (Figure B1), one of the dominant bivalve taxa in the Chukchi Sea, were collected at one station (CS12) on the Chukchi South line in the southern Chukchi Sea during the RUSALCA September 2012 expedi-tion. These specimens were used to estimate individual growth rates by measuring annual increments of carbonate added to their shells. To test the hypothesis that climatic factors have a significant impact on the growth of mollusks, the following climatic parameters were examined in relation to measured growth rates: a 10-year time series of bottom water temperatures observed from moorings in Bering Strait (Temp), the annual flux of incoming water flowing through Bering Strait (FW), the Arctic Oscillation (AO), and the Pacific/North American (PNA) pattern (Wallace and Gutzler, 1981; Woodgate et al., 2012).

We plotted individual mollusk growth increment curves (Figure  B2) and calculated a theoretical growth curve using the Gompertz formula (Bowers et  al., 1997). The Gompertz equation was used to describe the growth rates of the 40 individuals col-lected. This equation is based on growth rates (L), the growth coef-ficient (k), and the inflection point when growth rates change (i) (Table  B1). We also calculated the standardized growth rates of these mollusks, that is, the ratio of difference and derivative (RDD) (Denisenko, 2013). We determined that these standardized rates of growth for the mollusks collected (RDD) show long-term oscilla-tions (Figure B3).

Figure B1. The bivalve Yoldia hyperborea,

showing annual growth lines.

TABLE B1. Gompertz equation parameters used to approximate the growth of Yoldia hyperborea. Lx = maximum width of clams of this population, based upon model (theoretical), in mm). k = coefficient that describes growth rate (mm-1). I = inflection point where growth rates changed.

R2 L∞ ±95% k ±95% i ±95%

0.991 21.662 0.589 0.337 0.017 3.198 0.167

FIGURE  B2. Linear growth curves over time for 40 individual Yoldia hyperborea shells collected at one station (CS12) during the RUSALCA 2012 expe-dition in the Chukchi Sea.

FIGURE  B3. Time-series observations of the col-lected mollusks’ growth rates (RDD) showing a long-term oscillation of this parameter.

Oceanography | Vol.28, No.3154

0

4

8

12

16

20

24

2000 2002 2004 2006 2008 2010 2012 2014

–0.4

–0.2

0.0

0.2

0.4

0.6

0.8

1.0

2001 2003 2005 2007 2009 2011 2013

Obs

erve

d RD

D

Oceanography | September 2015 155

R2 = 0.717

0.55

0.60

0.65

0.70

0.75

0.80

0.85

0.50 0.60 0.70 0.80 0.90Predicted RDD

Obs

erve

d R

DD

–0.6

–0.3

0

0.3

0.6

0.9

1.2

2004 2005 2006 2007 2008 2009 2010 2011 2012

RDD RDD mod

–1.2

– 0.8

–0.4

0.0

0.4

0.8

1.2

2001 2003 2005 2007 2009 2011 2013

RDD AO

R² = 0.7436

–0.3

–0.1

0.1

0.3

0.5

0.7

0.9

–0.5 –0.2 0.1 0.4 0.7 1.0 1.3

Obs

erve

d

Predicted

TABLE B2. Summary of the ridge regression for the dependent variable standard-ized mollusk growth rates (RDD) using transformed data.

Adjusted R2 = 0.651, p < 0.025

Beta Std. Err. B Std. Err. p-level

Intercept 2.447 0.973 0.040

Temp 0.618 0.213 0.412 0.142 0.023

FW –0.464 0.213 –0.280 0.128 0.066

Correlation of Growth Rates with Climatic Parameters

The statistical analysis of the relationship between the growth rates of the 40 Y. hyperborea and climatic factors was carried out using correlation analysis, multiple regression analysis, and time series analysis. Multiple regression analysis was performed in two ways: stepwise multiple regressions and ridge multiple regressions (using Statistica 6). We used both raw data (untransformed) and transformed data (ln (x+2)) to determine the best approximation for the dependence of the growth rate on climatic variables. Significant correlations (p <0.05) were found between the transformed values of the RDD and water temperature and the AO (partial correlations are 0.680 and 0.674, respectively, for the transformed data).

As a result of multiple regression analysis undertaken in the model analysis, only one predictor—water temperature (Table B2)—provided satisfactory results with good agreement between pre-dicted and observed values (Figure B4). The initial data were treated as a time series and analyzed based on cross correlation between the RDD index and the climatic parameters. Figure B5 shows good coherence between the variability of the RDD and the AO indices. However, shifting the relationship of the standardized growth rate of Y. hyperborea (RDD) relative to the AO index provides a bet-ter match if a two-year delay (R2 = 0.782) is assumed (Table  B3, Figure B6). The relationship between observed RDD and modeled RDD also improves when a two-year lag is assumed between the AO and the RDD (Figure B7). The AO index is a measure of climatic influence, including water temperature (lag = one year, R2 = 0.903) and water flow (lag = two years, R2 = 0.964), as evidenced by the high values of the coefficient of determination. Therefore, we con-clude that the AO index is the most reliable predictor of standard-ized rate of growth for clams in this population (Figures B6 and B7).

FIGURE B6. Long-term dynamics of observed and predicted values of the mollusks’ growth rates (RDD) showing a two-year lag, which provides the best model agreement between the Arctic Oscillation and RDD.

FIGURE B4. Observed mollusk growth rates (RDD) vs. predicted RDD.

TABLE B3. Summary of distributed lags regression model.

Lag: 2 years, R2 = 0.782

Lag B Std. Err. p-level

0 –0.0287 0.1592 0.8630

1 0.2298 0.1550 0.1888

2 –0.7001 0.1721 *0.0066

FIGURE B7. Observed vs. predicted values of the mollusks’ growth rates (RDD) according to the dis-tributed two-year lag model.

FIGURE  B5. Comparison of long-term dynamics of the mollusks’ growth rates (RDD) to the Arctic Oscillation (AO).

Oceanography | September 2015 155

Oceanography | Vol.28, No.3156

trophic­feeding marine mammals such as walrus, time­series studies on spe­cific benthic animals, or at select sites (Grebmeier et  al., 2015b, in this issue), are needed. Finally, there are no data on the maximum life span or the average age of Nuculana radiata, Ennucula tenuis, and Psolus peroni, but, judging from their sizes in the Chukchi Sea, it is likely they also live for at least several years. The implication of these findings is that, on the large spatial scale, benthic popula­tions are stable, with slowly changing gen­erations (Neiman, 1988). Our studies, reported here, support previous classifica­tions of trophic characteristics and taxo­nomic structures of the benthic fauna of the Chukchi Sea. However, we see impacts of changing environmental conditions on bivalve growth rates (Box 1) and declin­ing bivalve biomass in the rich southern Chukchi Sea region (Grebmeier et  al., 2015b, in this issue). These two results suggest that although the overall ben­thic population structure may be stable on the large scale, small­scale studies are needed at specific sites to track the status of and changes in bivalve populations that are a critical component of the food web in the Chukchi Sea.

CONCLUSIONSChukchi Sea benthic ecosystems are among the most productive in the seas of the Russian and US sectors of the Arctic. The average biomass of zoobenthos in the Chukchi Sea is two times greater than in the Barents Sea. Because the Chukchi Sea is relatively shallow, pelagic­ benthic coupling of upper water column production is stronger than in the Barents Sea. Maximum values of zoobenthos bio­mass in the Chukchi Sea were found in the southern region due to a possible cyclonic gyre where seasonal changes in hydrodynamics can result in high pri­mary production, with phyto detritus being subsequently and efficiently exported to the underlying benthic com­munities. The persistence of this hydro­graphic feature is likely influenced by the northward flow of cold, nutrient­rich

Denisenko, S.G. 1997. Growth and life span of the commercial cockles in the southeastern Barents Sea. Pp. 36–37 in Non-Traditional Fishery Objects and Perspectives of Their Commercial Use. Abstracts of theoretical and practical conference, Murmansk. [in Russian]

Denisenko, S.G. 2002. Zoobenthos and ice dis-tribution in the Arctic seas. Proceedings of the Zoological Institute 296:39–46.

Denisenko, S.G. 2004. Structurally-functional char-acteristics of the Barents Sea zoobenthos. Proceedings of the Zoological Institute 300:43–52.

Denisenko, S.G. 2006. Multiannual fluctuation of zoobenthos in the Pechora Sea. Transactions of the Russian Geographical Society 138:37–48. [in Russian]

Denisenko, S.G. 2007. Barents Sea zoobenthos in conditions of changing climate and anthropo-genic impact. Pp. 418–511 in Dynamics of Marine Ecosystems and Modern Problems of Conservation of Biological Resources of the Russian Seas. V. Tarasov, ed., Dalnauka, Vladivostok. [in Russian]

Denisenko, S.G. 2013. Biodiversity and Bioresouces of Macrozoobenthos in the Barents Sea. Nauka, St. Petersburg, 284 pp. [in Russian]

Feder, H.M., S.C. Jewett, and A. Blanchard. 2005. Southeastern Chukchi Sea (Alaska) epibenthos. Polar Biology 28:402–421, http://dx.doi.org/10.1007/s00300-004-0683-4.

Feder, H.M., S.C. Jewett, and A. Blanchard. 2007. Southeastern Chukchi Sea (Alaska) macrobenthos. Polar Biology 30:261–275, http://dx.doi.org/10.1007/s00300-006-0180-z.

Gerasimova, A.V., and N.V. Maximovich. 2000. Analysis of long-term structural characteris-tics in the settlements of bivalve molluscs (White Sea area). Proceedings of the Saint-Petersburg University Series 3, 2(11):24–27. [in Russian]

Gorshkova, T.I. 1975. Organic matter in modern shelf deposits of the northern seas of the USSR. Pp. 66–72 in Problems of Shelf Geology. Nauka, Moscow. [in Russian]

Grebmeier, J.M. 1993. Studies of pelagic-benthic coupling extended onto the Soviet continen-tal shelf in the northern Bering and Chukchi Seas. Continental Shelf Research 13:653–658, http://dx.doi.org/10.1016/0278-4343(93)90098-I.

Grebmeier, J.M. 2012. Shifting patterns of life in the Pacific Arctic and sub-Arctic seas. Annual Review of Marine Science 4:63–78, http://dx.doi.org/ 10.1146/annurev-marine-120710-100926.

Grebmeier, J.M., B.A. Bluhm, L.W. Cooper, S.L. Danielson, K.R. Arrigo, A.L. Blanchard, J.T. Clarke, R.H. Day, K.E. Frey, R.R. Gradinger, and others. 2015a. Ecosystem characteristics and pro-cesses facilitating persistent macrobenthic biomass hotspots and associated benthivory in the Pacific Arctic. Progress in Oceanography 136:92–114, http://dx.doi.org/10.1016/j.pocean.2015.05.006.

Grebmeier, J.M., B.A. Bluhm, L.W. Cooper, S.G. Denisenko, K. Iken, M. Kędra, and C. Serratos. 2015. Time-series benthic community composition and biomass and associated environmental char-acteristics in the Chukchi Sea during the RUSALCA 2004–2012 Program. Oceanography 28(3):116–133, http://dx.doi.org/ 10.5670/ oceanog.2015.61.

Grebmeier, J.M., L.W. Cooper, M.H. Feder, and B.I. Sirenko. 2006a. Ecosystem dynamics of the Pacific influenced Bering and Chukchi Seas in the American Arctic. Progress in Oceanography 71:331–361, http://dx.doi.org/ 10.1016/j.pocean.2006.10.001.

Grebmeier, J.M., H.M. Feder, and C.P. McRoy. 1989. Pelagic-benthic coupling in the northern Bering and southern Chukchi Seas: Part II. Benthic com-munity structure. Marine Ecology Progress Series 51:253–268.

Pacific water, across­shelf differences in current speed, and variable bathymetric steering of these waters. Due to the result­ing deposition of large amounts of fresh phytodetritus to the benthos, the propor­tion of surface deposit feeders in the zoo­benthos is rather high, while that of fil­ter feeders is smaller than in the Barents Sea. Analysis of the spatial distribution of the key species may be useful not only for assessment of bioresources but also for studies of long­term fluctuations of zoo­benthos under the influence of various natural and anthropogenic factors.

REFERENCESAnonymous. 1985. Atlas of the Arctic. Glavnoe

upravlenie po geodezii i kartografii, Moscow, 204 pp. [in Russian]

Bigon, M., C.R. Townsend, and J.L. Harper. 2006. Ecology: From Individuals to Ecosystems, 4th ed. Wiley-Blackwell, 752 pp.

Blanchard, A.L., and H.M. Feder. 2014. Interactions of habitat complexity and environmental characteris-tics with macrobenthic community structure at mul-tiple spatial scales in the northeastern Chukchi Sea. Deep Sea Research Part II 102:132–143, http://dx.doi.org/10.1016/j.dsr2.2013.09.022.

Blanchard, A.L., C.L. Parris, A.L. Knowlton, and N.R. Wade. 2013a. Benthic ecology of the north-eastern Chukchi Sea: Part I. Environmental char-acteristics and macrofaunal community structure, 2008–2010. Continental Shelf Research 67:52–66, http://dx.doi.org/10.1016/j.csr.2013.04.021.

Blanchard, A.L., C.L. Parris, A.L. Knowlton, and N.R. Wade. 2013b. Benthic ecology of the north-eastern Chukchi Sea: Part II. Spatial vari-ation of megafaunal community structure, 2009–2010. Continental Shelf Research 67:67–76, http://dx.doi.org/10.1016/j.csr.2013.04.031.

Blokhin, S.A., and V.A. Pavluchkov. 1996. Foraging of grey whales in shallows off the Chukchi Peninsula in summer/autumn 1980. Transactions of the Pacific Fishery Research Centre 121:25–26. [in Russian]

Bowers, N.L., H.U. Gerber, J.C. Hickman, D.A. Jones, and C.J. Nesbitt. 1997. Actuarial Mathematics, 2nd ed. Society of Actuaries, Schaumburg, Illinois, 753 pp.

Brey, T. 2001. Population Dynamics in Benthic Invertebrates: A Virtual Handbook. Alfred Wegener Institute for Polar and Marine Research, Germany, http://www.thomas-brey.de/science/virtualhandbook/navlog/index.html.

Clarke, K.R, and R.M. Warwick. 2001. Change in Marine Communities: An Approach to Statistical Analysis and Interpolation, 2nd ed. PRIMER-E, Plymouth, UK, 168 pp.

Codispoti, L.A., V. Kelly, A. Thessen, P. Patrai, S. Suttles, V. Hill, M. Steele, and B. Light. 2013. Synthesis of primary production in the Arctic Ocean: Part III. Nitrate and phosphate based esti-mates of net community production. Progress in Oceanography 110:126–150, http://dx.doi.org/ 10.1016/j.pocean.2012.11.006.

Cooper, L.W., I.L. Larsen, J.M. Grebmeier, and S.B. Moran. 2005. Detection of rapid deposition of sea ice-rafted material to the Arctic Ocean ben-thos using the cosmogenic tracer 7Be. Deep Sea Research Part II 52:3,452–3,461, http://dx.doi.org/ 10.1016/j.dsr2.2005.10.011.

Oceanography | September 2015 157

Highsmith, R.C., K.O. Coyle, B.A. Bluhm, and B. Konar. 2006. Gray whales in the Bering and Chukchi Seas. Pp. 303–313 in Whales, Whaling and Ocean Ecosystems. J.A. Estes, D.P. Demaster, D.F. Doak, T.M. Williams, and R.L. Brownell Jr., eds, University of California Press, Santa Cruz.

Iken, K., B. Bluhm, and K. Dunton. 2010. Benthic food-web structure under differing water mass prop-erties in the southern Chukchi Sea. Deep Sea Research Part II 57(1):71–85, http://dx.doi.org/ 10.1016/j.dsr2.2009.08.007.

Illiashenko, V.Yu., and E.I. Illiashenko. 2000. Krasnaya kniga Rossii: Pravovye akty [Red Data Book of Russia: Legislative acts]. State Committee of the Russian Federation for Environmental Protection, Moscow. [in Russian]

Klyashtorin, L.B., and A.A. Lubushin. 2005. Cyclic Changes of Climate and Fish Productivity. VNIRO, Moscow, 235 pp. [in Russian]

Kortsch, S., R. Primicerio, F. Beuchel, P. Renaud, J. Rodrigues, O.J. Lønne, and B. Gulliksen. 2012. Climate-driven regime shifts in Arctic marine benthos. Proceedings of the National Academy of Sciences of the United States of America 109:14,052–14,057, http://dx.doi.org/ 10.1073/pnas.1207509109.

Kosheleva, V.A., and D.S. Yashin. 1999. Bottom Sediments of the Russian Arctic Seas. VNIIOkeangeologia, St. Petersburg, 286 pp. [in Russian]

Krause-Jensen, D., N. Marbà, B. Olsen, M.K. Sejr, P.B. Christensen, J.O. Rodrigues, P.E. Renaud, T.J.S. Balsby, and S. Rysgaard. 2012. Seasonal sea ice cover as principal driver of spatial and tempo-ral variation in depth extension and annual pro-duction of kelp in Greenland. Global Change Biology 18:2,981–2,994, http://dx.doi.org/ 10.1111/j.1365-2486.2012.02765.x.

Krylov, V.I. 1971. About foraging of the Pacific walrus (Odobenus rosmarus divergens III). Proceedings of AtlantNIRO 39:110–116. [in Russian]

Kuznetsov, A.P. 1980. Ecology of Bottom Communities of the World Ocean: Trophic Structure of Marine Bottom Fauna. Nauka, Moscow, 244 pp. [in Russian]

Kuznetsov, A.P. 1986. About deposit feeding and sus-pension feeding in class of the bivalve molluscs. Pp. 6–10 in Foraging of the Marine Invertebrates in Natural Conditions. M.N. Sokolova, ed., Institute of Oceanology of the USSR, Moscow. [in Russian]

Makarov, V.V. 1937. Materials on quantitative estima-tion of bottom fauna of the northern part of the Bering Sea and the Chukchi Sea. Explorations of the Seas of the USSR 25:260–291.

Möbius, K. 1877. Die Auster und die Austerwirtschaft. Berlin, 59 pp.

Moore, S.E., E. Logerwell, L. Eisner, E. Farley, L. Harwood, K. Kuletz, J. Lovvorn, J. Murphy, and L. Quakenbush. 2014. Marine fishes, birds and mammals as sentinels of ecosystem vari-ability and reorganization in the Pacific Arctic region. Pp. 337–392 in The Pacific Arctic Region: Ecosystem Status and Trends in a Rapidly Changing Environment. J.M. Grebmeier and W. Maslowski, eds, Springer, Dordrecht.

Münchow, A., T.J. Weingartner, and L.W. Cooper. 1999. The summer hydrography and surface cir-culation of the East Siberian Shelf Sea. Journal of Physical Oceanography 29:2,167–2,182, http://dx.doi.org/10.1175/1520-0485(1999)029 <2167%3ATSHASC>2.0.CO%3B2.

Neiman, A.A. 1961. Some patterns of ben-thos spatial distribution in the Bering Sea. Oceanology 1(2):294–304. [in Russian]

Neiman, A.A. 1988. Spatial Distribution and Trophic Structure of Benthos of the Wold Ocean Shelf. VNIRO, Moscow, 101 pp. [in Russian]

Petersen, G.H. 1978. Life cycles and population dynamics of marine benthic bivalves from the Disko Bugt area of West Greenland. Ophelia 17(1):95–120, http://dx.doi.org/10.1080/00785326.1978.10425475.

Pearson, T.H., and R. Rosenberg. 1978. Macrobenthic succession in relation to organic enrich-ment and pollution of the marine environment. Oceanography and Marine Biology: An Annual Review 16:229–311.

Pianka, E.R. 1994. Evolutionary Ecology, 5th ed. HarperCollins, New York, 411 pp.

Pickart, R.S., M.A. Spall, and J.T. Mathis. 2013. Dynamics of upwelling in the Alaskan Beaufort Sea and associated shelf-basin fluxes. Deep Sea Research Part I 76:35–51, http://dx.doi.org/10.1016/ j.dsr.2013.01.007.

Piraino, S., S. Fanelli, and F. Boero. 2002. Variability of species’ roles in marine communities: Change of paradigms for conservation priorities. Marine Biology 140:1,067–1,074, http://dx.doi.org/10.1007/s00227-001-0769-2.

Pisareva, M.N., R.S. Pickart, K. Iken, E.A. Ershova, J.M. Grebmeier, L.W. Cooper, B.A. Bluhm, C. Nobre, R.R. Hopcroft, H. Hu, and others. 2015. The rela-tionship between patterns of benthic fauna and zooplankton in the Chukchi Sea and physical forc-ing. Oceanography 28(3):68–83, http://dx.doi.org/ 10.5670/oceanog.2015.58.

Ratmanov, G.E. 1937. The hydrology of the Bering and Chukchi seas. Explorations of the Far-East Seas 5:10–118. [in Russian]

Rusanova, M.N. 1963. Short information on [Summaries of?] the biology of some common species of invertebrates from the area of Cape Kartesh. Materials on Complex Exploration of the White Sea. 2:53–65. [in Russian]

Sakshaug, E. 2004. Primary and secondary pro-duction in Arctic Seas. P. 57–81 in The Organic Carbon Cycle in the Arctic Ocean. R. Stein and R.W. Macdonald, eds, Springer, Berlin.

Schlitzer, R. 2015. Ocean Data View, http://odv.awi.de.Sheffield, G., and J.M. Grebmeier. 2009. Pacific

walrus (Odobenus rosmarus divergens): Differential prey digestion and diet. Marine Mammal Science 25:761–777, http://dx.doi.org/ 10.1111/j.1748-7692.2009.00316.x.

Shuntov, V.P. 2001. Biology of Russian Far-East Seas. TINRO-tsentr, Vladivostok, 580 pp.

Sirenko, B.I., S.G. Denisenko, S.Ju. Gagaev, A.N. Golikov, A.A. Golikov, and V.V. Petrjshev. 2009. Bottom communities of the Chukchi Sea shelf at depths below 10 m. Pp. 32–55 in Ecosystems and Bioresources of the Chukchi Sea and Adjacent Waters. B.I. Sirenko ed., Explorations of the Seas 64(72), ZIN RAS, St. Petersburg.

Sirenko, B.I., and S.Ju. Gagaev. 2007. Unusual abundance of macrozoobenthos and Pacific invaders in the Chukchi Sea based of the first RUSALCA expedition. Russian Journal of Marine Biology 33(6):399–407.

Sirenko, B.I., and V.M. Koltun. 1992. Characteristics of benthic biocenoses of the Chukchi and Bering Seas. Pp. 251–258 in Results of the Third Joint US–USSR Bering and Chukchi Seas Expedition (BERPAC): Summer 1988. J.F. Turner and P.A. Nagel, eds, US Fish and Wildlife Service, Washington, DC.

Stoker, S.W. 1978. Benthic invertebrate macrofauna of the eastern continental shelf of the Bering/Chukchi Seas. Dissertation, University of Alaska Fairbanks.

Vorobyev, V.P. 1949. Benthos of the Azov Sea. Proceedings of AzCherNIRO, vol. 13, 193 pp. [in Russian]

Wallace, J.M., and D.S. Gutzler. 1981. Teleconnections in the geopotential height field during the Northern Hemisphere winter. Monthly Weather Review 109(4):784–812, http://dx.doi.org/10.1175/ 1520-0493(1981)109<0784:TITGHF>2.0.CO;2.

Wassmann, P., M. Reigstad, T. Haug, B. Rudels, M. Carroll, H. Hop, G. Gabrielsen, S. Falk-Petersen, S.G. Denisenko, E. Arashkevich, and others. 2006. Food webs and carbon flux in the Barents Sea. Progress in Oceanography 71:232–287, http://dx.doi.org/10.1016/j.pocean.2006.10.003.

Weingartner, T., K. Aagaard, R. Woodgate, S. Danielson, Y. Sasaki, and D. Cavalieri. 2005. Circulation on the north central Chukchi Sea shelf. Deep Sea Research Part II 52:3,150–3,174, http://dx.doi.org/10.1016/j.dsr2.2005.10.015.

Whittaker, R. 1975. Communities and Ecosystems. Macmillan, New York, 352 pp.

Woodgate, R.A., T.J. Weingartner, and R. Lindsay. 2012. Observed increases in Bering Strait oceanic fluxes from the Pacific to the Arctic from 2001 to 2011 and their impacts on the Arctic Ocean water column. Geophysical Research Letters 39, L24603, http://dx.doi.org/10.1029/2012GL054092.

Zenkevich, L.A. 1951. Seas of the USSR, Their Fauna and Flora. Uchpedgis, Moscow. 368 pp.

ACKNOWLEDGMENTS The authors are thankful to Boris Sirenko, Sergey Gagayev, Viktor Petryashev, Peter Strelkov, Vladimir Skvortsov, Vyacheslav Dzhurinskiy, and Aleksey Merkulyev for zoobenthos sampling in 2004 and 2006, and sampling assistance in 2009 and 2012. We also thank Arianne Balsom (2004) and Betty Carvellas (2009 and 2012) for field col-lections for the Grebmeier/Cooper RUSALCA com-ponent. Financial support was provided by the National Oceanic and Atmospheric Administration (NOAA) Arctic Office to PIs Grebmeier and Cooper (2004: NOAA-CIFAR 10-067, 2004-2005; 2009 and 2012: NA08OAR4310608), and by the RUSALCA synthesis award (NOAA Cooperative Agreement #NA09OAR4320129: WHOI CINAR #19930.00 UMCES).

AUTHORSStanislav G. Denisenko (stanislav.denisenko@zin.ru) is Professor, Zoological Institute, Russian Academy of Sciences, St. Petersburg, Russia. Jacqueline M. Grebmeier is Research Professor, Chesapeake Biological Laboratory, University of Maryland Center for Environmental Science, Solomons, MD, USA. Lee W. Cooper is Research Professor, Chesapeake Biological Laboratory, University of Maryland Center for Environmental Science, Solomons, MD, USA.

BOX AUTHORSStanislav G. Denisenko is at the Zoological Institute, Russian Academy of Sciences, St. Petersburg, Russia. Vladimir V. Skvortsov is at the Herzen State Pedogogical University of Russia, St. Petersburg, Russia.

ARTICLE CITATIONDenisenko, S.G., J.M. Grebmeier, and L.W. Cooper. 2015. Assessing bioresources and standing stock of zoobenthos (key species, high taxa, trophic groups) in the Chukchi Sea. Oceanography 28(3):146–157, http://dx.doi.org/10.5670/oceanog.2015.63.